Much stronger coarse-to-fine visual processing in primate superior colliculus than primary visual cortex neurons

Abstract

The visual system optimizes its signal processing properties to efficiently encode natural scenes. The superior colliculus (SC) and primary visual cortex (V1) both play important roles in visual-motor processing, and they both exhibit qualitatively similar visual responses. However, it is not clear whether the SC simply inherits V1s efficient coding image processing optimizations or not, especially given that the SC receives a substantial amount of direct anatomical inputs from V1. Here, by performing matched experiments in the two brain areas, as well as with the same visual stimuli and in the same experimental animals, we show that the dynamics of coarse-to-fine visual image processing in the SC are much stronger than those in V1. In the SC, visual response latencies, being fastest for coarse patterns, are dictated by image spatial frequency, independently of the spatial frequency tuning curves of the neurons. On the other hand, V1 visual response latencies are largely dominated by visual response sensitivity, which is itself much more broadband than in the SC. These observations remain fundamentally unchanged in active vision gaze-shift scenarios eliciting visual reafferent responses in both brain areas. Our results suggest that coarse-to-fine visual image processing dynamics are most observable, and thus most relevant, in visually-responsive neurons driving foveating eye movements, like in the SC. Besides explaining behavioral evidence for saccadic facilitation by images that are consistent with the statistics of natural scenes, these results indicate that coarse-to-fine visual processing dynamics are much more of a collicular than a cortical visual phenomenon.